Termination of the geniculocortical projection in the striate cortex of macaque monkey: A quantitative immunoelectron microscopic study

Latawiec, Diane; Martin, Kevan A; Meskenaïte, Virginia

doi:10.1002/(sici)1096-9861(20000410)419:3<306::aid-cne4>3.0.co;2-2

Cited by 74 publications

(59 citation statements)

References 68 publications

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“…This is a small number of synapses, Ͻ10% of the asymmetric synapses that SSs are expected to receive (Beaulieu and Colonnier, 1985;Anderson et al, 1994;Binzegger et al, 2004), and is comparable to previous estimates for cat visual cortex: 80 -100 (Binzegger et al, 2004), 100 -125 (Peters and Payne, 1993), and 286 (Ahmed et al, 1994). The number of thalamocortical synapses per neuron is also small for the primate visual cortex:18 -188 synapses (Peters et al, 1994;Latawiec et al, 2000). By contrast Bruno and Sakmann (2006) estimated that there were ϳ600 synapses per neuron in the rat barrel cortex, although they have since revised this number down to ϳ90 -580 synapses per layer 4 neuron (Meyer et al, 2010).…”

Section: Discussionsupporting

confidence: 82%

How Thalamus Connects to Spiny Stellate Cells in the Cat's Visual Cortex

Costa¹,

Martin²

2011

J. Neurosci.

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In the cat's visual cortex, the responses of simple cells seem to be totally determined by their thalamic input, yet only a few percent of the excitatory synapses in layer 4 arise from the thalamus. To resolve this discrepancy between structure and function, we used correlated light and electron microscopy to search individual spiny stellate cells (simple cells) for possible structural features that would explain the biophysical efficacy of the thalamic input, such as synaptic location on dendrites, size of postsynaptic densities, and postsynaptic targets. We find that thalamic axons form a small number of synapses with the spiny stellates (188 on average), that the median size of the synapses is slightly larger than that of other synapses on the dendrites of spiny stellates, that they are not located particularly proximal to the soma, and that they do not cluster on the dendrites. These findings point to alternative mechanisms, such as synchronous activation of the sparse thalamic synapses to boost the efficacy of the thalamic input. The results also support the idea that the thalamic input does not by itself determine the cortical response of spiny stellate cells, allowing the cortical microcircuit to amplify and modulate its response according to the particular context and computation being performed.

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Section: Discussionsupporting

confidence: 82%

How Thalamus Connects to Spiny Stellate Cells in the Cat's Visual Cortex

Costa¹,

Martin²

2011

J. Neurosci.

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“…However, it does not seem to be the quantity of synapses alone, but their quality that relates to an increase in CO activity, given the fact that thalamic afferents account for only ϳ5% of the total amount of excitatory synapses in layer IV in V1 of cats (Ahmed et al, 1994). For layer IVc of V1 of the macaque, a thalamic proportion of ϳ5-10% of all synapses was reported by Garey and Powell (1971), and Latawiec et al (2000) estimate that parvocellular afferents build ϳ8% of all asymmetric synapses there. In V2, thick and pale stripes receive afferents from the same source in V1 (Sincich and Horton, 2002) with the pale stripes in fact getting most of these.…”

Section: Discussionmentioning

confidence: 99%

Vascularization of Cytochrome Oxidase-Rich Blobs in the Primary Visual Cortex of Squirrel and Macaque Monkeys

Keller¹,

Schüz²,

Logothetis³

et al. 2011

J. Neurosci.

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The close correlation between energy supply by blood vessels and energy consumption by cellular processes in the brain is the basis of blood flow-related functional imaging techniques. Regional differences in vascular density can be detected using high-resolution functional magnetic resonance imaging. Therefore, inhomogeneities in vascularization might help to identify anatomically distinct areas noninvasively in vivo. It was reported previously that cytochrome oxidase-rich blobs in the striate cortex of squirrel monkeys are characterized by a notably higher vascular density (42% higher than interblob regions). However, blobs have so far never been identified in vivo on the basis of their vascular density. Here, we analyzed blobs of the primary visual cortex of squirrel monkeys and macaques with respect to the relationship between vascularization and cytochrome oxidase activity. By double staining with cytochrome oxidase enzyme histochemistry to define the blobs and collagen type IV immunohistochemistry to quantify the blood vessels, a close correlation between oxidative metabolism and vascularization was confirmed and quantified in detail. The vascular length density in cytochrome oxidase blobs was on average 4.5% higher than in the interblob regions, a difference almost one order of magnitude smaller than previously reported. Thus, the vascular density that is closely associated with local average metabolic activity is a structural equivalent of cerebral metabolism and blood flow. However, the quantitative differences in vascularization between blob and interblob regions are small and below the detectability threshold of the noninvasive hemodynamic imaging methods of today.

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“…First, our sampling of excitatory synapses excluded the VGlut2-containing thalamocortical excitatory synapses (51). However, previous EM studies demonstrated that thalamic excitatory inputs represent only ∼10% of total excitatory synapses in the cortex (52) and only a small percentage (∼2%) of thalamic inputs innervate PV interneurons (53). Second, we excluded sampling of synapses on the dendrites of PV interneurons in monkey DLPFC due to the lack of PV immunoreactivity within these structures.…”

Section: Phospho-erbb4mentioning

confidence: 99%

Developmental pruning of excitatory synaptic inputs to parvalbumin interneurons in monkey prefrontal cortex

Chung

Wills

Fish

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Working memory requires efficient excitatory drive to parvalbuminpositive (PV) interneurons in the primate dorsolateral prefrontal cortex (DLPFC). Developmental pruning eliminates superfluous excitatory inputs, suggesting that working memory maturation during adolescence requires pruning of excitatory inputs to PV interneurons. Therefore, we tested the hypothesis that excitatory synapses on PV interneurons are pruned during adolescence. The density of excitatory synapses, defined by overlapping vesicular glutamate transporter 1-positive (VGlut1+) and postsynaptic density 95-positive (PSD95+) puncta, on PV interneurons was lower in postpubertal relative to prepubertal monkeys. In contrast, puncta levels of VGlut1 and PSD95 proteins were higher in postpubertal monkeys and positively predicted activity-dependent PV levels, suggesting a greater strength of the remaining synapses after pruning. Because excitatory synapse number on PV interneurons is regulated by erb-b2 receptor tyrosine kinase 4 (ErbB4), whose function is influenced by alternative splicing, we tested the hypothesis that pruning of excitatory synapses on PV interneurons is associated with developmental shifts in ErbB4 expression and/or splicing. Pan-ErbB4 expression did not change, whereas the minor-to-major splice variant ratios increased with age. In cell culture, the major, but not the minor, variant increased excitatory synapse number on PV interneurons and displayed greater kinase activity than the minor variant, suggesting that the effect of ErbB4 signaling in PV interneurons is mediated by alternative splicing. Supporting this interpretation, in monkey DLPFC, higher minor-to-major variant ratios predicted lower PSD95+ puncta density on PV interneurons. Together, our findings suggest that ErbB4 splicing may regulate the pruning of excitatory synapses on PV interneurons during adolescence.synaptic pruning | parvalbumin interneuron | ErbB4 | alternative splicing | schizophrenia I n primates, certain complex cognitive processes, such as working memory, depend in part on the proper activation of specific neural circuits in the dorsolateral prefrontal cortex (DLPFC) (1). In both monkeys and humans, recruitment of DLPFC activity and performance during working memory tasks continue to improve through adolescence (2-4). During this period, excitatory synapses and their principal targets, pyramidal neuron dendritic spines, massively decline in number in the primate DLPFC (5-8). Synaptic pruning is thought to eliminate unwanted or imprecise connections and to strengthen the remaining connections (9, 10), suggesting that this process could contribute to the maturation of working memory function during adolescence.Working memory is thought to emerge from oscillatory activity of DLPFC neurons at gamma frequency (30-80 Hz) (11), which requires the activity of local GABAergic interneurons that express the calcium binding protein parvalbumin (PV) (12, 13). During working memory tasks, excitation from pyramidal neurons recruits PV interneurons, which in turn pro...

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Termination of the geniculocortical projection in the striate cortex of macaque monkey: A quantitative immunoelectron microscopic study

Cited by 74 publications

References 68 publications

How Thalamus Connects to Spiny Stellate Cells in the Cat's Visual Cortex

How Thalamus Connects to Spiny Stellate Cells in the Cat's Visual Cortex

Vascularization of Cytochrome Oxidase-Rich Blobs in the Primary Visual Cortex of Squirrel and Macaque Monkeys

Developmental pruning of excitatory synaptic inputs to parvalbumin interneurons in monkey prefrontal cortex

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